T-cell landscape in a primary melanoma predicts the survival of patients with metastatic disease after their treatment with dendritic cell vaccines

Cancer Research

Volumn 76, Issue 12, 2016, Pages 3496-3506

  Vasaturo, Angela ^a   Halilovic, Altuna ^a,b   Bol, Kalijn F ^a,b   Verweij, Dagmar I ^a,b   Blokx, Willeke A M ^b   Punt, Cornelis J A ^c   Groenen, Patricia J T A ^b   Van Krieken, J Han J M ^b   Textor, Johannes ^a,d   De Vries, I Jolanda M ^a,b   Figdor, Carl G ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DACARBAZINE; DENDRITIC CELL VACCINE; LACTATE DEHYDROGENASE; CANCER VACCINE;

ADULT; AGED; ARTICLE; CANCER CHEMOTHERAPY; CANCER PROGNOSIS; CANCER STAGING; CD3+ T LYMPHOCYTE; CUTANEOUS MELANOMA; FEMALE; HUMAN; HUMAN TISSUE; LACTATE DEHYDROGENASE BLOOD LEVEL; LYMPHOCYTIC INFILTRATION; MAJOR CLINICAL STUDY; MALE; METASTATIC MELANOMA; MULTIPLE CYCLE TREATMENT; PRIORITY JOURNAL; SURVIVAL TIME; T LYMPHOCYTE; DENDRITIC CELL; IMMUNOLOGY; MELANOMA; METASTASIS; MORTALITY; TUMOR ASSOCIATED LEUKOCYTE; VACCINATION;

CANCER VACCINES; DENDRITIC CELLS; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA; NEOPLASM METASTASIS; T-LYMPHOCYTES; VACCINATION;

EID: 84976907921     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-3211     Document Type: Article

References (44)

1. Erdmann F, Lortet-Tieulent J, Schuz J, Zeeb H, Greinert R, Breitbart EW, et al. International trends in the incidence of malignant melanoma 1953-2008 - are recent generations at higher or lower risk? Int J Cancer 2013;132:385-400.
2. Balch CM, Gershenwald JE, Soong SJ, Thompson JF, Atkins MB, Byrd DR, et al. Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol 2009;27:6199-206.
3. Palathinkal DM, Sharma TR, Koon HB, Bordeaux JS. Current systemic therapies for melanoma. Dermatol Surg 2014;40:948-63.
4. Sharma P, Allison JP. Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential. Cell 2015;161:205-14.
5. Kelderman S, Heemskerk B, van Tinteren H, van den Brom RR, Hospers GA, van den Eertwegh AJ, et al. Lactate dehydrogenase as a selection criterion for ipilimumab treatment in metastatic melanoma. Cancer Immunol Immunother 2014;63:449-58.
6. Fridman WH, Pages F, Sautes-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 2012;12:298-306.
7. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011;331:1565-70.
8. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006;313:1960-4.
9. Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 2003;348:203-13.
10. Liu H, Zhang T, Ye J, Li H, Huang J, Li X, et al. Tumor-infiltrating lymphocytes predict response to chemotherapy in patients with advance non-small cell lung cancer. Cancer Immunol Immunother 2012;61:1849-56.
11. Clark WHJr, Elder DE, Guerry Dt, Braitman LE, Trock BJ, Schultz D, et al. Model predicting survival in stage I melanoma based on tumor progression. J Natl Cancer Inst 1989;81:1893-904.
12. Azimi F, Scolyer RA, Rumcheva P, Moncrieff M, Murali R, McCarthy SW, et al. Tumor-infiltrating lymphocyte grade is an independent predictor of sentinel lymph node status and survival in patients with cutaneous melanoma. J Clin Oncol 2012;30:2678-83.
13. Clemente CG, Mihm MCJr, Bufalino R, Zurrida S, Collini P, Cascinelli N. Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer 1996;77:1303-10.
14. Bogunovic D, O'Neill DW, Belitskaya-Levy I, Vacic V, Yu YL, Adams S, et al. Immune profile and mitotic index of metastatic melanoma lesions enhance clinical staging in predicting patient survival. Proc Natl Acad Sci U S A 2009;106:20429-34.
15. Taylor RC, Patel A, Panageas KS, Busam KJ, Brady MS. Tumor-infiltrating lymphocytes predict sentinel lymph node positivity in patients with cutaneous melanoma. J Clin Oncol 2007;25:869-75.
16. Mandala M, Imberti GL, Piazzalunga D, Belfiglio M, Labianca R, Barberis M, et al. Clinical and histopathological risk factors to predict sentinel lymph node positivity, disease-free and overall survival in clinical stages I-II AJCC skin melanoma: outcome analysis from a single-institution prospectively collected database. Eur J Cancer 2009;45:2537-45.
17. Burton AL, Roach BA, Mays MP, Chen AF, Ginter BA, Vierling AM, et al. Prognostic significance of tumor infiltrating lymphocytes in melanoma. Am Surg 2011;77:188-92.
18. Karagiannis P, Fittall M, Karagiannis SN. Evaluating biomarkers in melanoma. Front Oncol 2014;4:383.
19. Lesterhuis WJ, Aarntzen EH, De Vries IJ, Schuurhuis DH, Figdor CG, Adema GJ, et al. Dendritic cell vaccines in melanoma: from promise to proof? Crit Rev Oncol Hematol 2008;66:118-34.
20. Jacobs JF, Punt CJ, Lesterhuis WJ, Sutmuller RP, Brouwer HM, Scharenborg NM, et al. Dendritic cell vaccination in combination with anti-CD25 monoclonal antibody treatment: a phase I/II study in metastatic melanoma patients. Clin Cancer Res 2010;16:5067-78.
21. Tel J, Aarntzen EH, Baba T, Schreibelt G, Schulte BM, Benitez-Ribas D, et al. Natural human plasmacytoid dendritic cells induce antigen-specific T-cell responses in melanoma patients. Cancer Res 2013;73:1063-75.
22. Wilgenhof S, Van Nuffel AM, Benteyn D, Corthals J, Aerts C, Heirman C, et al. A phase IB study on intravenous synthetic mRNA electroporated dendritic cell immunotherapy in pretreated advanced melanoma patients. Ann Oncol 2013;24:2686-93.
23. Anguille S, Smits EL, Lion E, van Tendeloo VF, Berneman ZN. Clinical use of dendritic cells for cancer therapy. Lancet Oncol 2014;15:e257-67.
24. de Vries IJ, Bernsen MR, Lesterhuis WJ, Scharenborg NM, Strijk SP, Gerritsen MJ, et al. Immunomonitoring tumor-specific T cells in delayed-type hypersensitivity skin biopsies after dendritic cell vaccination correlates with clinical outcome. J Clin Oncol 2005;23:5779-87.
25. Aarntzen EH, Bol K, Schreibelt G, Jacobs JF, Lesterhuis WJ, van Rossum MM, et al. Skin-test infiltrating lymphocytes early predict clinical outcome of dendritic cell based vaccination in metastatic melanoma. Cancer Res 2012;72:6102-10.
26. Wimmers F, Aarntzen EH, Schreibelt G, Jacobs JF, Ja Punt C, Figdor CG, et al. Early predictive value of multifunctional skin-infiltrating lymphocytes in anticancer immunotherapy. Oncoimmunology 2014;3:e27219.
27. Lesterhuis WJ, de Vries IJ, Schreibelt G, Lambeck AJ, Aarntzen EH, Jacobs JF, et al. Route of administration modulates the induction of dendritic cell vaccine-induced antigen-specific T cells in advanced melanoma patients. Clin Cancer Res 2011;17:5725-35.
28. Lesterhuis WJ, Schreibelt G, Scharenborg NM, Brouwer HM, Gerritsen MJ, Croockewit S, et al. Wild-type and modified gp100 peptide-pulsed dendritic cell vaccination of advanced melanoma patients can lead to longterm clinical responses independent of the peptide used. Cancer Immunol Immunother 2011;60:249-60.
29. Aarntzen EH, Schreibelt G, Bol K, Lesterhuis WJ, Croockewit AJ, de Wilt JH, et al. Vaccination with mRNA-electroporated dendritic cells induces robust tumor antigen-specific CD4+ and CD8+ T cells responses in stage III and IV melanoma patients. Clin Cancer Res 2012;18:5460-70.
30. Aarntzen EH, De Vries IJ, Lesterhuis WJ, Schuurhuis D, Jacobs JF, Bol K, et al. Targeting CD4(+) T-helper cells improves the induction of antitumor responses in dendritic cell-based vaccination. Cancer Res 2013;73:19-29.
31. Bol KF, Figdor CG, Aarntzen EH, Welzen ME, van Rossum MM, Blokx WA, et al. Intranodal vaccination with mRNA-optimized dendritic cells in metastatic melanoma patients. Oncoimmunology 2015;4:e1019197.
32. Mansfield JR. Cellular context in epigenetics: quantitative multicolor imaging and automated per-cell analysis of miRNAs and their putative targets. Methods 2010;52:271-80.
33. Stack EC, Wang C, Roman KA, Hoyt CC. Multiplexed immunohistochemistry, imaging, and quantitation: a review, with an assessment of Tyramide signal amplification, multispectral imaging and multiplex analysis. Methods 2014;70:46-58.
34. Hansen BB, Klopfer SO. Optimal full matching and related designs via network flows. J Comput Graph Stat 2006;15:609-27.
35. Gajewski TF, Louahed J, Brichard VG. Gene signature in melanoma associated with clinical activity: a potential clue to unlock cancer immunotherapy. Cancer J 2010;16:399-403.
36. Hamid O, Schmidt H, Nissan A, Ridolfi L, Aamdal S, Hansson J, et al. A prospective phase II trial exploring the association between tumor microenvironment biomarkers and clinical activity of ipilimumab in advanced melanoma. J Transl Med 2011;9:204.
37. Mahoney KM, Atkins MB. Prognostic and predictive markers for the new immunotherapies. Oncology 2014;28Suppl 3:39-48.
38. Taube JM, Klein A, Brahmer JR, Xu H, Pan X, Kim JH, et al. Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy. Clin Cancer Res 2014;20:5064-74.
39. Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 2014;515:568-71.
40. Madore J, Vilain RE, Menzies AM, Kakavand H, Wilmott JS, Hyman J, et al. PD-L1 expression in melanoma shows marked heterogeneity within and between patients: implications for anti-PD-1/PD-L1 clinical trials. Pigment Cell Melanoma Res 2015;28:245-53.
41. Bol KF, Aarntzen EH, Hout FE, Schreibelt G, Creemers JH, Lesterhuis WJ, et al. Favorable overall survival in stage III melanoma patients after adjuvant dendritic cell vaccination. Oncoimmunology 2015;5:e1057673.
42. Eggermont AM, Chiarion-Sileni V, Grob JJ, Dummer R, Wolchok JD, Schmidt H, et al. Adjuvant ipilimumab versus placebo after complete resection of high-risk stage III melanoma (EORTC 18071): a randomised, double-blind, phase 3 trial. Lancet Oncol 2015;16:522-30.
43. Tjin EP, Krebbers G, Meijlink KJ, van de Kasteele W, Rosenberg EH, Sanders J, et al. Immune-escape markers in relation to clinical outcome of advanced melanoma patients following immunotherapy. Cancer Immunol Res 2014;2:538-46.
44. de Moll EH, Fu Y, Qian Y, Perkins SH, Wieder S, Gnjatic S, et al. Immune biomarkers are more accurate in prediction of survival in ulcerated than in non-ulcerated primary melanomas. Cancer Immunol Immunother 2015;64:1193-203.